Clinical potential of electroporation for gene therapy and DNA vaccine delivery

Bibliography

Papers of special note have been highlighted as 

• of interest

•• of considerable interest

• Kaestner L, Scholz A, Lipp P. Conceptual and technical aspects of transfection and gene delivery. Bioorg Med Chem Lett. 2015;25(6):1171–1176.
   PubMed Web of Science ®Google Scholar
• Mali B, Jarm T, Snoj M, et al. Antitumor effectiveness of electrochemotherapy: a systematic review and meta-analysis. Eur J Surg Oncol. 2013;39(1):4–16.
   PubMed Web of Science ®Google Scholar
• Yarmush ML, Golberg A, Sersa G, et al. Electroporation-based technologies for medicine: principles, applications, and challenges. Annu Rev Biomed Eng. 2014;16:295–320.
   PubMed Web of Science ®Google Scholar

• This book gives a very complete overview of all electroporation (EP)-based technologies in clinic.

• Denet AR, Vanbever R, Preat V. Skin electroporation for transdermal and topical delivery. Adv Drug Deliv Rev. 2004;56(5):659–674.
   PubMed Web of Science ®Google Scholar
• Bennett WF, Sapay N, Tieleman DP. Atomistic simulations of pore formation and closure in lipid bilayers. Biophys J. 2014;106(1):210–219.
   PubMed Web of Science ®Google Scholar
• Rols MP. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim Biophys Acta. 2006;1758(3):423–428.
   PubMed Web of Science ®Google Scholar
• Teissie J, Golzio M, Rols MP. Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of ?) knowledge. Biochim Biophys Acta. 2005;1724(3):270–280.
   PubMed Web of Science ®Google Scholar
• Gothelf A, Gehl J. What you always needed to know about electroporation based DNA vaccines. Hum Vacc Immunother. 2012;8(11):1694–1702.
   PubMed Web of Science ®Google Scholar
• Marszalek P, Liu DS, Tsong TY. Schwan equation and transmembrane potential induced by alternating electric field. Biophys J. 1990;58(4):1053–1058.
   PubMed Web of Science ®Google Scholar

• First study to indicate that the Schwan equation may be used to describe the transmembrane potential of a living cell generated by an oscillating electric field.

• Kotnik T, Pucihar G, Miklavcic D. Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport. J Membr Biol. 2010;236(1):3–13.
   PubMed Web of Science ®Google Scholar
• Kotnik T, Pucihar G. Induced transmembrane voltage - theory, modeling, and experiments. In: Pakhomov AG, Miklavcic D, Markov MS, editors. Advanced electroporation techniques in biology and medicine. Boca Raton (FL): CRC Press; 2010.
   Google Scholar

•• The book was edited by experts and pioneers in the field of electroporation and details experimental findings, biophysical theories and application in biomedical research of EP.

• Kotnik T, Frey W, Sack M, et al. Electroporation-based applications in biotechnology. Trends Biotechnol. 2015;33(8):480–488.
   PubMed Web of Science ®Google Scholar
• Miklavcic D, Beravs K, Semrov D, et al. The importance of electric field distribution for effective in vivo electroporation of tissues. Biophys J. 1998;74(5):2152–2158.
   PubMed Web of Science ®Google Scholar
• Hirao LA, Wu L, Khan AS, et al. Intradermal/subcutaneous immunization by electroporation improves plasmid vaccine delivery and potency in pigs and rhesus macaques. Vaccine. 2008;26(3):440–448.
   PubMed Web of Science ®Google Scholar
• Wells DJ. Gene therapy progress and prospects: Electroporation and other physical methods. Gene Ther. 2004;11(18):1363–1369.
   PubMed Web of Science ®Google Scholar
• Bolhassani A, Khavari A. Orafa Z electroporation – advantages and drawbacks for delivery of drug, gene and vaccine. In: Sezer AD, editor. Nanotechnology in drug delivery. Rijeka: InTech; 2014.
   Google Scholar

• This is an excellent overview about the history of EP, its mechanism and its applications for drug and vaccine delivery and for gene therapy.

• Gehl J. Gene electrotransfer in clinical trials. Methods Mol Biol. 2014;1121:241–246.
   PubMedGoogle Scholar
• Heller LC, Heller R. In vivo electroporation for gene therapy. Human Gene Therapy. 2006;17(9):890–897.
   PubMed Web of Science ®Google Scholar
• Senovilla L, Vacchelli E, Garcia P, et al. Trial watch: DNA vaccines for cancer therapy. Oncoimmunology. 2013;2(4):e23803.
   PubMed Web of Science ®Google Scholar
• Kobiyama K, Jounai N, Aoshi T, et al. Innate Immune Signaling by, and Genetic Adjuvants for DNA Vaccination. Vaccines. 2013;1(3):278.
   Google Scholar
• Babiuk S, Baca-Estrada ME, Foldvari M, et al. Increased gene expression and inflammatory cell infiltration caused by electroporation are both important for improving the efficacy of DNA vaccines. J Biotechnol. 2004;110(1):1–10.
   PubMed Web of Science ®Google Scholar
• Chiarella P, Massi E, De Robertis M, et al. Electroporation of skeletal muscle induces danger signal release and antigen-presenting cell recruitment independently of DNA vaccine administration. Expert Opin Biol Ther. 2008;8(11):1645–1657.
   PubMed Web of Science ®Google Scholar
• Weaver JC. Electroporation theory Concepts and mechanisms. Methods Mol Biol. 1995;55:3–28.
   PubMedGoogle Scholar
• Andreason G. Electroporation as a technique for the transfer of macromolecules into mammalian cell lines. J Tissue Culture Methods. 1993;15(2):56–62.
   Google Scholar
• Staal L, Gilbert R. Generators and applicators: equipment for electroporation. In: Kee ST, Gehl J, Lee EW, editors. Clinical aspects of electroporation. New York (NY): Springer; 2011. p. 45–65.
   Google Scholar

•• The book gives an overview of the basic principles behind the development of EP and its introduction into clinical practice.

• Heller R, Heller LC. Gene electrotransfer clinical trials. Adv Genet. 2015;89:235–262.
   PubMed Web of Science ®Google Scholar
• El-Kamary SS, Billington M, Deitz S, et al. Safety and Tolerability of the Easy Vax™ Clinical Epidermal Electroporation System in Healthy Adults. Mol Ther. 2012;20(1):214–220.
   PubMed Web of Science ®Google Scholar
• Spanggaard I, Snoj M, Cavalcanti A, et al. Gene electrotransfer of plasmid antiangiogenic metargidin peptide (AMEP) in disseminated melanoma: safety and efficacy results of a phase I first-in-man study. Hum Gene Ther Clin Dev. 2013;24(3):99–107.
   PubMed Web of Science ®Google Scholar

• The first report about the use of pAMEP, an antiangiogenic plasmid, in clinical trial for treating cutaneous melanoma.

• Eriksson F, Tötterman T, Maltais A-K, et al. DNA vaccine coding for the rhesus prostate specific antigen delivered by intradermal electroporation in patients with relapsed prostate cancer. Vaccine. 2013;31(37):3843–3848.
   PubMed Web of Science ®Google Scholar
• Wallace M, Evans B, Woods S, et al. Tolerability of Two Sequential Electroporation Treatments Using MedPulser DNA Delivery System (DDS) in Healthy Adults. Mol Ther J Am Soc Gene Ther. 2009;17(5):922–928.
   PubMed Web of Science ®Google Scholar
• Diehl MC, Lee JC, Daniels SE, et al. Tolerability of intramuscular and intradermal delivery by CELLECTRA(®) adaptive constant current electroporation device in healthy volunteers. Hum Vacc Immunother. 2013;9(10):2246–2252.
   PubMed Web of Science ®Google Scholar

• The first published clinical study about the tolerability of CELLECTRA, the second most used EP device in clinical trials.

• Vasan S, Hurley A, Schlesinger SJ, et al. In vivo electroporation enhances the immunogenicity of an HIV-1 DNA vaccine candidate in healthy volunteers. PLoS One 2011;6(5):e19252.
   PubMed Web of Science ®Google Scholar

• Shows the outcomes of the first clinical trial using the TriGrid delivery system, which is nowadays the most used EP device in clinical trials.

• Yuan J, Ku GY, Adamow M, et al. Immunologic responses to xenogeneic tyrosinase DNA vaccine administered by electroporation in patients with malignant melanoma. J Immunother Cancer. 2013;1:20–20.
   PubMedGoogle Scholar
• Kim TJ, Jin H-T, Hur S-Y, et al. Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients. Nat Commun. 2014;5:5317.
   PubMed Web of Science ®Google Scholar
• Kalams SA, Parker SD, Elizaga M, et al. Safety and comparative immunogenicity of an HIV-1 DNA vaccine in combination with plasmid interleukin 12 and impact of intramuscular electroporation for delivery. J Infect Dis. 2013;208(5):818–829.
   PubMed Web of Science ®Google Scholar
• Mpendo J, Mutua G, Nyombayire J, et al. A Phase I Double Blind, Placebo-Controlled, Randomized Study of the Safety and Immunogenicity of Electroporated HIV DNA with or without Interleukin 12 in Prime-Boost Combinations with an Ad35 HIV Vaccine in Healthy HIV-Seronegative African Adults. PLoS One. 2015;10(8):e0134287.
   PubMed Web of Science ®Google Scholar
• Weiland O, Ahlen G, Diepolder H, et al. Therapeutic DNA vaccination using in vivo electroporation followed by standard of care therapy in patients with genotype 1 chronic hepatitis C. Mol Ther. 2013;21(9):1796–1805.
   PubMed Web of Science ®Google Scholar
• Hooper JW, Moon JE, Paolino KM, et al. A Phase 1 clinical trial of Hantaan virus and Puumala virus M-segment DNA vaccines for haemorrhagic fever with renal syndrome delivered by intramuscular electroporation. Clin Microbiol Infect. 2014;20(Suppl 5):110–117.
   PubMed Web of Science ®Google Scholar
• Yang B, Jeang J, Yang A, et al. DNA vaccine for cancer immunotherapy. Hum Vaccin Immunother. 2014;10(11):3153–3164.
   PubMed Web of Science ®Google Scholar
• Bagarazzi ML, Yan J, Morrow MP, et al. Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses. Sci Transl Med. 2012;4(155):155ra38.
   Web of Science ®Google Scholar
• Trimble CL, Morrow MP, Kraynyak KA, et al. Safety, efficacy, and immunogenicity of VGX-3100, a therapeutic synthetic DNA vaccine targeting human papillomavirus 16 and 18 E6 and E7 proteins for cervical intraepithelial neoplasia 2/3: a randomised, double-blind, placebo-controlled phase 2b trial. Lancet. 2015;386(10008):2078–2088.
   Web of Science ®Google Scholar
• Lucas ML, Heller L, Coppola D, et al. IL-12 plasmid delivery by in vivo electroporation for the successful treatment of established subcutaneous B16.F10 melanoma. Mol Ther. 2002;5(6):668–675.
   PubMed Web of Science ®Google Scholar
• Daud AI, DeConti RC, Andrews S, et al. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol. 2008;26(36):5896–5903.
   PubMed Web of Science ®Google Scholar
• Welch M, Villalobos A, Gustafsson C, et al. You’re one in a googol: optimizing genes for protein expression. J Royal Soc Interface. 2009;6(Suppl 4):S467–S76.
   Google Scholar
• Plotkin JB, Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet. 2011;12(1):32–42.
   PubMed Web of Science ®Google Scholar
• Angov E. Codon usage: Nature’s roadmap to expression and folding of proteins. Biotechnol J. 2011;6(6):650–659.
   PubMed Web of Science ®Google Scholar
• Kotsopoulou E, Kim VN, Kingsman AJ, et al. A Rev-Independent Human Immunodeficiency Virus Type 1 (HIV-1)-Based Vector That Exploits a Codon-Optimized HIV-1 gag-pol Gene. J Virol. 2000;74(10):4839–4852.
   PubMed Web of Science ®Google Scholar
• Li L, Saade F, Petrovsky N. The future of human DNA vaccines. J Biotechnol. 2012;162(2–3):171–182.
   PubMed Web of Science ®Google Scholar
• Saade F, Petrovsky N. Technologies for enhanced efficacy of DNA vaccines. Expert Rev Vaccines. 2012;11(2):189–209.
   PubMed Web of Science ®Google Scholar
• Papadakis ED, Nicklin SA, Baker AH, et al. Promoters and control elements: designing expression cassettes for gene therapy. Curr Gene Ther. 2004;4(1):89–113.
   PubMed Web of Science ®Google Scholar
• Vandermeulen G, Richiardi H, Escriou V, et al. Skin-specific promoters for genetic immunisation by DNA electroporation. Vaccine. 2009;27(32):4272–4277.
   PubMed Web of Science ®Google Scholar
• Danda R, Krishnan G, Ganapathy K, et al. Targeted expression of suicide gene by tissue-specific promoter and microRNA regulation for cancer gene therapy. Plos One. 2013;8(12):e83398.
   Google Scholar
• Kos S, Tesic N, Kamensek U, et al. Improved specificity of gene electrotransfer to skin using pDNA under the control of collagen tissue-specific promoter. J Membr Biol. 2015;248(5):919–928.
   PubMed Web of Science ®Google Scholar
• Bode C, Zhao G, Steinhagen F, et al. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines. 2011;10(4):499–511.
   PubMed Web of Science ®Google Scholar
• Tudor D, Dubuquoy C, Gaboriau V, et al. TLR9 pathway is involved in adjuvant effects of plasmid DNA-based vaccines. Vaccine. 2005;23(10):1258–1264.
   PubMed Web of Science ®Google Scholar
• Babiuk S, Mookherjee N, Pontarollo R, et al. TLR9-/- and TLR9+/+ mice display similar immune responses to a DNA vaccine. Immunology. 2004;113(1):114–120.
   PubMed Web of Science ®Google Scholar
• Vandermeulen G, Marie C, Scherman D, et al. New Generation of Plasmid Backbones Devoid of Antibiotic Resistance Marker for Gene Therapy Trials. Mol Ther. 2011;19(11):1942–1949.
   PubMed Web of Science ®Google Scholar
• Okuda K, Wada Y, Shimada M. Recent Developments in Preclinical DNA Vaccination. Vaccines. 2014;2(1):89.
   PubMedGoogle Scholar
• Grunwald T, Ulbert S. Improvement of DNA vaccination by adjuvants and sophisticated delivery devices: vaccine-platforms for the battle against infectious diseases. Clin Exp Vaccine Res. 2015;4(1):1–10.
   PubMed Web of Science ®Google Scholar
• Weiss JM, Subleski JJ, Wigginton JM, et al. Immunotherapy of cancer by IL-12-based cytokine combinations. Expert Opin Biol Ther. 2007;7(11):1705–1721.
   PubMed Web of Science ®Google Scholar
• Dinarello CA. Proinflammatory cytokines. Chest. 2000;118(2):503–508.
   PubMed Web of Science ®Google Scholar
• Flingai S, Czerwonko M, Goodman J, et al. Synthetic DNA vaccines: improved vaccine potency by electroporation and co-delivered genetic adjuvants. Front Immunol. 2013;4:354.
   PubMed Web of Science ®Google Scholar
• Scheerlinck JY. Genetic adjuvants for DNA vaccines. Vaccine. 2001;19(17–19):2647–2656.
   PubMed Web of Science ®Google Scholar
• Sersa G, Teissie J, Cemazar M, et al. Electrochemotherapy of tumors as in situ vaccination boosted by immunogene electrotransfer. Cancer Immunol Immunother. 2015;64(10):1315–1327.
   PubMed Web of Science ®Google Scholar
• Vandermeulen G, Vanvarenberg K, De Beuckelaer A, et al. The site of administration influences both the type and the magnitude of the immune response induced by DNA vaccine electroporation. Vaccine. 2015;33(28):3179–3185.
   PubMed Web of Science ®Google Scholar
• Gothelf A, Gehl J. Gene electrotransfer to skin; review of existing literature and clinical perspectives. Curr Gene Ther. 2010;10(4):287–299.
   PubMed Web of Science ®Google Scholar
• Gothelf A, Mahmood F, Dagnaes-Hansen F, et al. Efficacy of transgene expression in porcine skin as a function of electrode choice. Bioelectrochemistry. 2011;82(2):95–102.
   PubMed Web of Science ®Google Scholar
• Maruyama H, Ataka K, Higuchi N, et al. Skin-targeted gene transfer using in vivo electroporation. Gene Ther. 2001;8(23):1808–1812.
   PubMed Web of Science ®Google Scholar
• Daugimont L, Baron N, Vandermeulen G, et al. Hollow Microneedle Arrays for Intradermal Drug Delivery and DNA Electroporation. J Membrane Biol. 2010;236(1):117–125.
   PubMed Web of Science ®Google Scholar
• Sersa G, Miklavcic D, Cemazar M, et al. Electrochemotherapy in treatment of tumours. Ejso-Eur J Surg Onc. 2008;34(2):232–240.
   PubMed Web of Science ®Google Scholar
• Heller R, Cruz Y, Heller LC, et al. Electrically mediated delivery of plasmid DNA to the skin, using a multielectrode array. Human Gene Therapy. 2010;21(3):357–362.
   PubMed Web of Science ®Google Scholar
• Guo SQ, Donate A, Basu G, et al. Electro-gene transfer to skin using a noninvasive multielectrode array. J Control Release. 2011;151(3):256–262.
   PubMed Web of Science ®Google Scholar
• Drabick JJ, Glasspool-Malone J, Somiari S, et al. Cutaneous transfection and immune responses to intradermal nucleic acid vaccination are significantly enhanced by in vivo electropermeabilization. Mol Ther. 2001;3(2):249–255.
   PubMed Web of Science ®Google Scholar
• Donate A, Coppola D, Cruz Y, et al. Evaluation of a Novel Non-Penetrating Electrode for Use in DNA Vaccination. Plos One. 2011;6:4.
   Web of Science ®Google Scholar
• Pavselj N, Preat V. DNA electrotransfer into the skin using a combination of one high- and one low-voltage pulse. J Control Release. 2005;106(3):407–415.
   PubMed Web of Science ®Google Scholar
• Roos AK, Eriksson F, Walters DC, et al. Optimization of Skin Electroporation in Mice to Increase Tolerability of DNA Vaccine Delivery to Patients. Mol Ther. 2009;17(9):1637–1642.
   PubMed Web of Science ®Google Scholar
• Andre FM, Gehl J, Sersa G, et al. Efficiency of High- and Low-Voltage Pulse Combinations for Gene Electrotransfer in Muscle, Liver, Tumor, and Skin. Human Gene Therapy. 2008;19(11):1261–1271.
   PubMed Web of Science ®Google Scholar
• Rabussay D, Dev NB, Fewell J, et al. Enhancement of therapeutic drug and DNA delivery into cells by electroporation. J Phys D Appl Phys. 2003;36(4):348–363.
   Web of Science ®Google Scholar
• Rabussay D, Widera G, Zhang L, et al. Toward the development of electroporation for delivery of DNA vaccines to humans. Mol Ther. 2004;9:S209–S09.
   Google Scholar
• Groselj A, Kos B, Cemazar M, et al. Coupling treatment planning with navigation system: a new technological approach in treatment of head and neck tumors by electrochemotherapy. Biomed Eng Online. 2015;14(Suppl 3):S2.
   Google Scholar
• Calvet CY, Famin D, Andre FM, et al. Electrochemotherapy with bleomycin induces hallmarks of immunogenic cell death in murine colon cancer cells. Oncoimmunology. 2014;3:e28131.
   PubMed Web of Science ®Google Scholar
• Yang FQ, Yu YY, Wang GQ, et al. A pilot randomized controlled trial of dual-plasmid HBV DNA vaccine mediated by in vivo electroporation in chronic hepatitis B patients under lamivudine chemotherapy. J Viral Hepat. 2012;19(8):581–593.
   PubMed Web of Science ®Google Scholar
• Kim CY, Kang ES, Kim SB, et al. Increased in vivo immunological potency of HB-110, a novel therapeutic HBV DNA vaccine, by electroporation. Exp Mol Med. 2008;40(6):669–676.
   PubMed Web of Science ®Google Scholar